brainsciences

Article

Language Problems and ADHD Symptoms: HowSpecific Are the Links?

Erin Hawkins *, Susan Gathercole, Duncan Astle, The CALM Team and Joni Holmes

MRC Cognition and Brain Sciences Unit, Cambridge, CB2 7EF, UK; susan.gathercole@mrc-cbu.cam.ac.uk (S.G.);duncan.astle@mrc-cbu.cam.ac.uk (D.A.); joni.holmes@mrc-cbu.cam.ac.uk (J.H.)* Correspondence: erin.hawkins@mrc-cbu.cam.ac.uk; Tel.: +44-1-223-273-686

Academic Editor: Paul E. EngelhardtReceived: 16 July 2016; Accepted: 14 October 2016; Published: 21 October 2016

Abstract: Symptoms of inattention and hyperactivity frequently co-occur with language difficultiesin both clinical and community samples. We explore the specificity and strength of these associationsin a heterogeneous sample of 254 children aged 5 to 15 years identified by education and healthprofessionals as having problems with attention, learning and/or memory. Parents/carers ratedpragmatic and structural communication skills and behaviour, and children completed standardisedassessments of reading, spelling, vocabulary, and phonological awareness. A single dimension ofbehavioural difficulties including both hyperactivity and inattention captured behaviour problems.This was strongly and negatively associated with pragmatic communication skills. There was lessevidence for a relationship between behaviour and language structure: behaviour ratings weremore weakly associated with the use of structural language in communication, and there were nolinks with direct measures of literacy. These behaviour problems and pragmatic communicationdifficulties co-occur in this sample, but impairments in the more formal use of language that impacton literacy and structural communication skills are tied less strongly to behavioural difficulties.One interpretation is that impairments in executive function give rise to both behavioural and socialcommunication problems, and additional or alternative deficits in other cognitive abilities impact onthe development of structural language skills.

Keywords: ADHD; attention; hyperactivity; learning; language; communication

1. Introduction

Symptoms of inattention and hyperactivity typically co-occur with poor communicationskills [1,2] and low levels of literacy [3–5] in children with attention deficit hyperactivity disorder(ADHD). The same comorbidities are also found in the general school population [6,7] and in otherneurodevelopmental conditions including autism spectrum disorder (ASD) [8], specific languageimpairment (SLI) [9], and dyslexia [10,11]. These overlapping symptom profiles may reflect dimensionsof inattentive and hyperactive behaviour and cognitive difficulties that cut across traditional diagnosticcategories [12–14]. In the current study we adopt a dimensional approach to test the specificity ofthe associations between these dimensions of behaviour, communication and literacy skills in a largesample of children receiving support from specialist services for difficulties in attention, learningand/or memory. The sample included a small number of children with diagnosed developmentaldisorders and a substantial number with sub-clinical difficulties. The atypical and heterogeneousnature of the sample enabled us to investigate the extent to which impairments in language andbehaviour co-occurred in children with problems related to educational progress.

Difficulties in both the formal learning of language structure and the use of language in differentcontexts are common in developmental disorders [1,15–17]. Structural aspects of language includethe use of phonology, semantics, syntax and morphology. These skills are important for literacy

Brain Sci. 2016, 6, 50; doi:10.3390/brainsci6040050 www.mdpi.com/journal/brainsci

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development [18,19] and for expressing and understanding spoken language in communication [20].Pragmatic aspects of language involve the appropriate use of language in social communicativecontexts such as maintaining appropriate topics, not talking excessively, turn-taking in conversationsand interpreting non-verbal cues of others [21,22]. It is unclear whether impairments in pragmaticlanguage arise as a secondary consequence of structural language problems [23] or instead reflectsocial or behavioural difficulties [7,24]. Evidence that children can have pragmatic language difficultiesin the absence of problems with language structure supports the view that these two dimensions oflanguage impairment may have different sources [22,25].

Profiles of structural and pragmatic language difficulties differ across specific diagnostic groups.For example, pragmatic language impairments are common in high-functioning autism [16] andADHD [1,6,21,26], but structural language difficulties are more common in children with readingdifficulties and SLI [12,14,27]. However, there is also considerable heterogeneity within each diagnosticcategory, as demonstrated for example by the prevalence of pragmatic language difficulties amongchildren with SLI [28]. There is also substantial overlap between the linguistic profiles of children withdifferent diagnoses, illustrated by the prevalence of pragmatic language difficulties in both childrenwith ADHD and those with autism [1]. These two groups also show elevated symptoms of bothinattention and hyperactivity typically common in both disorders [29–31], illustrating how symptomprofiles of language and behaviour problems may not be specific to particular disorders.

Pragmatic communication problems are also associated with the severity of symptoms ofinattention and hyperactivity in other clinical and typically developing populations [1,6,21]. A possiblesource of these co-morbid problems are the executive function difficulties frequently observed inchildren with attentional symptoms of ADHD [32,33]. It has been suggested that ADHD may arise fromdisruptions to two functionally distinct neurodevelopmental systems: cool cognitive-based functionsthat include working memory, planning, and inhibition, and which are associated with inattention;and hot affective processes that are associated with delay aversion and impulsive behaviours [34].Effective pragmatic communication may also rely on both of these systems. Cool cognitive functionsmay be required to maintain information about the conversational topic and to produce coherent,well-planned and appropriate conversational speech [2,35,36], whilst affective processes may berequired for appropriate turn taking, and to limit excessive talking [2,37]. Deficits in one or both ofthese dimensions may therefore impair pragmatic communication and cause problems with socialand peer relationships [7,38]. Consistent with this, research has shown that children with elevatedsymptoms of inattention and hyperactivity have intact knowledge of pragmatics but problems in theexecutive skills needed to apply it in social contexts [2,6,39].

Impairments in language structure also co-occur with ADHD symptoms across differentpopulations. Deficits in structural components of communication such as the use of syntax andphonology are present in children with ADHD [2]. Weak literacy skills are also associated withboth elevated levels of inattention and hyperactivity in clinical and community samples [40–44],with stronger links with inattention [45–48]. A possible explanation for this association is thatbehavioural inattention disrupts the formal acquisition of reading skills through its impact onclassroom behaviour, which reduces children’s ability to attend to direct instructions required forlearning to read [49]. This model is supported by evidence that preschool inattention predicts laterreading skills independently from other early markers of literacy development such as phonemeawareness and letter knowledge [40,41,50]. Difficulties paying attention may also have a directeffect on the development of structural language skills that are important for literacy development(e.g., phonological processing) [51–53]. An alternative possibility is that underlying deficits in executivefunctions such as working memory underlie both short attention spans and literacy problems [3,32,33].

Pragmatic and structural language problems encompassing poor structural communication andliteracy therefore co-occur with the symptoms of ADHD, but evidence for the specificity and strengthsof these relationships is mixed. To date, studies have focused on either diagnosed groups or communitysamples containing large numbers of typically developing children. The present study explored the

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relationship between these dimensions of impairment across diagnostic categories in a unique sampleof struggling learners. The children had difficulties in attention, learning, or memory, and werereceiving support from professionals working in children’s services, including speech and languagetherapists, educational psychologists, school-based special educational needs co-ordinators, mentalhealth practitioners, and paediatricians. Approximately one third had received formal diagnoses(e.g., of ADHD, ASD, or dyslexia) and the remainder had sub-clinical difficulties of varying severity.Based on previous findings of an association between behavioural problems and pragmatic languagedifficulties we expected behaviour problems to be more highly linked with pragmatic than structurallanguage skills overall, with additional specific associations between behavioural inattention andassessments of structural language skills in literacy.

Assessments included standardised tests of reading, spelling, phonological awareness andvocabulary, as well as parent ratings of children’s behaviour and pragmatic and structuralcommunication skills. Because of the atypicality of this sample, a data driven approach was usedto examine the relationships between behaviour and language skills. We sought to identify whetherseparate dimensions of inattentive and hyperactive behaviour problems were present in the sample,and the extent to which these behaviours were related to poor structural and pragmatic language skills.

2. Method

2.1. Participants

Participants were recruited from an ongoing study at the Cambridge Centre for Attention,Learning, and Memory (CALM) based in the MRC Cognition and Brain Sciences Unit in Cambridge,UK. Children were referred to the CALM research clinic for problems in one or more areas of attention,learning, and memory. The current sample consisted of the first 254 children seen in the clinic forwhom there were complete data. The age range of the sample was 5:5–15:11 (M = 9:4, SD = 2:3),with 169 males and 85 females. No diagnosis was reported for the majority of the sample (n = 191).Twenty children had a diagnosis of ADHD, and a further 59 children had been identified with otherdevelopmental learning disorders (e.g., dyslexia, dyscalculia, autism spectrum disorders) or psychiatricdiagnoses (see Table 1). Exclusion criteria for referrals to the clinic were: (i) significant and severeknown problems in vision or hearing that are uncorrected; and (ii) a native language other than English.Ethical approval was provided by the Local NHS Research Ethics Committee, reference 13/EE/0157.Written informed consent was obtained from parents/guardians, and informed verbal assent wasobtained from children.

2.2. Procedure

Children completed a battery of tests on a one-to-one basis with a researcher in a dedicatedchild-friendly testing room at the CALM clinic. These included a wide range of standardisedassessments of learning and cognition. Regular breaks were included throughout the session. Testingwas split over two sessions for children who struggled to complete the assessments in one sitting.Parents/carers completed a set of questionnaires relating to behaviour, learning, communication,and medical and family history in a family waiting area while their child was assessed. Measures ofbehaviour, communication skills, and literacy are reported here.

2.3. Measures

Behaviour

Parent ratings of behaviour

The Conners 3 Parent Short Form [54] is a questionnaire assessing behavioural and cognitiveproblems related to ADHD. Parents or caregivers rated 45 items as not true at all (0); just a little true(1); pretty much true (2); or very much true (4). Scores on these items formed six subscales consisting

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of Inattention, Hyperactivity, Learning Problems, Executive Function, Aggression, and Peer Relations.The sum of raw scores on each subscale was converted to a T-score (M = 50, SD = 10) for a normativesample 6:00–18:00 years of age. If children’s age fell outside the standardisation range the closestage match was used. T-scores ≥70 on an individual subscale indicate the child has very elevatedbehavioural problems for their age. T-scores 60–69 are within the elevated range, scores 40–59 arein the average range, and scores ≤39 indicate a child has fewer reported problems than average fortheir age.

Table 1. Sample referral and diagnoses.

Referrer Male Female Total

SENCo 103 58 161Specialist Teacher 8 5 13

Educational Psychologist 4 2 6Speech and Language Therapist 13 9 22

Clinical Psychologist 13 7 20Paediatrician 22 4 26

Diagnosis Male Female Total

None 105 59 164ADD 2 2 4

ADHD 16 4 20ASD 11 1 12

DAMP 2 1 3Depression 0 2 2Dysgraphia 1 0 1

Dyslexia 13 5 18Dyspraxia 6 3 9

FASD 1 2 3Generalised Developmental Delay 1 1 2

Global Delay, Dyspraxia 1 0 1Hyperactivity 1 0 1

OCD 0 1 1Social Anxiety Disorder, Depression 0 1 1

Tourettes 1 0 1

Primary Reason for Referral Male Female Total

Attention 34 12 46Literacy 30 11 41Maths 6 3 9

Language 16 7 23Poor academic progress 53 41 94

Memory 20 8 28Anxiety 1 0 1

Note. The following datapoints were missing: Referral route, 6 data points; Diagnosis, 11 data points;Primary Reason for Referral, 12 datapoints. Abbreviations: SENCo–Special Educational Needs Coordinator;ADD–Attention Deficit Disorder; ADHD–Attention Deficit Hyperactivity Disorder; ASD–Autism SpectrumDisorder; DAMP–Deficits in Attention and Motor Perception; FASD–Fetal Alcohol Spectrum Disoder;OCD–Obsessive Compulsive Disorder.

2.4. Literacy

2.4.1. Reading

The Single-Word Reading subtest on the Wechsler Individual Achievement Test II (WIAT-II) [55]assessed children’s reading abilities. Children read a list of words aloud that were scored by theexaminer. Responses were coded as correct if they were pronounced correctly and fluently. Standardscores (M = 100, SD = 15) were derived from the raw scores, with a normative sample age range of4:00–16:11.

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2.4.2. Spelling

The Spelling sub-test on the WIAT-II provided a measure of spelling attainment. Children wereasked to spell words spoken one at a time by the examiner. Raw scores were converted to standardscores (M = 100, SD = 15) with a normative sample 4:00–16:11 years of age.

2.4.3. Vocabulary

The Peabody Picture Vocabulary Test, Fourth Edition (PPVT-4) [56] assessed receptive vocabularyknowledge. Children were required to select one of four pictures showing the meaning of a spokenword. Standard scores were calculated (M = 100, SD = 15), and the normative sample had an age rangeof 2:6–90:00.

2.4.4. Phonological awareness

The Alliteration subtest of the Phonological Assessment Battery (PhAB) [57] tested phonologicalawareness. Sets of three spoken words were read aloud and children were required to judge whichtwo words started with the same sound. The number of correct responses formed raw scores, whichwere converted to standardised scores (M = 100, SD = 15). Children who were too young or unableto complete the Alliteration subtest were given the Alliteration Test with Pictures subtest. In thisversion children saw pictures corresponding to words named aloud by the researcher. Children hadto indicate which two pictures corresponded to words starting with the same sound. Raw scores onthe Alliteration Test with Pictures were converted to standardised scores (M = 100, SD = 15). If achild’s age fell outside the standardisation range (6:00–14:11) the closest age match was used to obtaina standardised score.

2.5. Communication

The Children’s Communication Checklist, second edition (CCC-2) [58] was used to measurecommunication skills. This 70-item questionnaire assessed language structure and form, and verbaland nonverbal pragmatic communication. Scaled scores (M = 10, SD = 3) were derived for 10 subscalesthat fell into three categories measuring different aspects of language use. The first four scaleswere (A) Speech; (B) Syntax; (C) Semantics; and (D) Coherence. These assessed language structure,vocabulary use, and discourse, and are areas of communication typically impaired in children with SLI.The next four scales were (E) Inappropriate Initiation; (F) Stereotyped Language; (G) Use of Context;and (H) Nonverbal Communication. These indexed verbal and nonverbal pragmatic communicationskills. The final two scales, (I) Social relations; and (J) Interests, assessed aspects of language behaviourthat are usually impaired in ASD. Clinically significant communication impairments on the CCC-2 areinterpreted using percentiles rather than scaled scores. Scores below the 15th percentile, correspondingapproximately to a scaled score of 6, are considered below normal limits (see [58] for further details).For the present purposes, scaled scores ≤6 are considered as corresponding to deficits. The normativesample had an age range of 4:0–16:11.

3. Results

3.1. Analysis Plan

To characterise our sample we first compared performance on each measure to the age-normedpopulation mean, calculated the proportion of children in the deficit range on each measure, andchecked for gender differences in performance. The following Bonferroni corrected significancethresholds were used to correct for multiple comparisons: behaviour, p < 0.008; communication,p < 0.005; literacy, p < 0.0125.

To assess the specificity and strength of links between ADHD behaviours and languageskills we first conducted correlation analyses between each measure individual measure. Next,

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we used exploratory factor analysis (EFA) to reduce the dimensionality of the data and identifythe underlying constructs of language and behaviour. One EFA was conducted for the behaviourmeasure. The language measures were entered into two separate EFAs, one for the parent/carerratings of communication and another for the direct assessments of literacy. Principal axis factoringwith direct Oblimin rotation was used to allow factors to be correlated. Factors were chosen based onan eigenvalue cut-off of 1 and examination of the scree plots.

Resulting factor scores were correlated to explore the associations between different dimensionsof impairment. Partial correlations were also computed that controlled for age. The relative strength ofthe associations between each pair of factors was tested using Meng’s Z test, which is used to comparecorrelation coefficients [59]. For all analyses involving the communication data, scores were excludedfor children whose CCC-2 ratings were identified as invalid due to disproportionately negative orpositive responses [58].

3.2. Descriptive Statistics

Descriptive statistics are presented in Table 2. Relative to standardised age-norms, the samplehad significantly poorer language and communication skills, and significantly elevated behaviouralproblems across all of the measures. Comparison of standard scores indicated that children hadsubstantially more behaviour problems, poorer spoken communication and poorer reading, spelling,and phonological skills. This is to be expected given how the sample was recruited. Independentt-tests comparing scores for males and females on each measure indicated gender differences only onthe literacy measures of vocabulary and phonological skills, in which males scored higher. No genderdifferences were present across the behaviour and communication measures, or in the literacy measuresof reading and spelling.

3.3. Correlational Analyses

Correlations between the behaviour and communication measures are presented in Table 3.The majority of the behaviour measures showed a significant negative correlation with thecommunication measures, indicating that children with poorer behaviour had weaker communicationskills. Correlations between Inattention and Speech, and between Executive Function, Speech andSyntax, were not significant.

Table 4 shows the correlations between behaviour and the literacy measures. Literacy skillswere negatively associated with ratings of Learning Problems, showing that children rated as poorerlearners had lower scores on the direct measures of literacy skills. There were no other significantrelationships between behavioural difficulties and literacy.

The correlations between the literacy and communication measures are presented in Table 5.Reading, spelling, and vocabulary were positively correlated with the majority of the communicationmeasures, indicating that children rated as having better communication skills performed better onthese direct assessments of literacy. Phonological awareness was positively correlated only with theparent-rated structural communication scales of speech, syntax, and semantics.

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Table 2. Sample descriptive statistics.

Whole Sample Gender Split

N Mean SD EffectSize †

Percentage ofChildren in

Deficit RangeSkewness Kurtosis Male

Mean SD FemaleMean SD t p d

Age in months 254 111.830 26.804 111.69 26.746 112.12 27.075 −0.119 0.905 −0.016

Behaviour (Conners)Inattention 253 78.522 12.281 2.560 88.9 −0.978 −0.014 79.435 11.468 76.718 13.640 1.576 0.117 0.216Hyperactivity 254 70.413 16.098 1.564 71.3 −0.293 −1.230 71.864 15.934 67.529 16.127 2.037 0.043 0.270Learning Problems 254 76.228 12.017 2.383 89.8 −0.540 −0.789 74.929 12.132 78.812 11.420 −2.454 0.015 −0.330Executive Function 254 72.047 13.235 1.898 81.5 −0.412 −0.767 72.308 12.412 71.529 14.801 0.417 0.678 0.057Aggression 254 60.961 16.778 0.819 43.7 0.668 −1.036 61.615 16.773 59.659 16.811 0.877 0.382 0.117Peer Relations 254 70.421 18.708 1.423 63.4 −0.377 −0.979 71.811 18.639 67.659 18.646 1.675 0.095 0.223

Communication (CCC-2)Speech 248 5.528 3.991 −1.279 61.7 0.300 −1.056 5.484 3.948 5.863 4.217 −0.663 0.508 −0.093Syntax 248 5.436 4.131 −1.280 63.9 0.340 −1.083 5.369 4.021 5.849 4.462 −0.813 0.417 −0.113Semantics 248 4.492 3.421 −1.716 76.5 0.873 0.302 4.331 3.350 4.932 3.713 −1.222 0.223 −0.170Coherence 248 4.682 3.017 −1.768 75.7 0.741 0.506 4.618 3.083 4.822 3.133 −0.465 0.642 −0.066Inappropriate initiation 248 6.077 3.053 −1.296 57.4 0.509 0.057 5.834 3.065 6.507 3.056 −1.550 0.122 −0.220Stereotyped language 246 6.155 3.401 −1.202 53.9 0.300 −0.528 6.089 3.483 6.380 3.437 −0.587 0.558 −0.084Use of context 248 4.617 3.630 −1.624 72.6 0.733 0.076 4.612 3.770 4.822 3.645 −0.398 0.691 −0.057Nonverbal communication 248 5.371 3.520 −1.420 64.3 0.499 −0.392 5.312 3.614 5.534 3.363 −0.443 0.658 −0.064Social relations 248 5.488 4.128 −1.266 58.7 0.278 −1.141 5.229 4.255 6.356 4.087 −1.893 0.060 −0.270Interests 248 6.137 2.939 −1.301 61.7 0.828 0.866 5.847 2.820 6.890 3.247 −2.487 0.014 −0.344

LiteracyReading 253 85.455 17.354 −0.899 50.2 0.103 −0.449 86.148 17.989 84.060 16.012 0.901 0.368 0.123Spelling 251 82.406 15.111 −1.169 62.2 −0.293 3.217 82.249 15.911 82.732 13.400 −0.237 0.813 −0.033Vocabulary 250 97.172 15.631 −0.185 22.0 −0.315 1.330 99.898 14.949 91.687 15.618 4.030 0.000 ** 0.537Alliteration 251 90.697 10.044 −0.743 32.3 −0.616 −0.823 92.132 9.393 87.845 10.724 3.112 0.002 ** 0.426

Note. † The effect size of the difference between the normative sample mean and the current sample mean. The deficit range on each measure was scores falling more than 1 SD belowthe normative sample mean. ** denotes significance at the 0.01 level, two-tailed.

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Table 3. Correlations between behaviour ratings and communication subscales.

Measure 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15

1. Inattention2. Hyperactivity/impulsivity 0.573 **

3. Learning problems 0.324 ** 0.172 **4. Executive function 0.596 ** 0.419 ** 0.330 **

5. Aggression 0.338 ** 0.530 ** 0.197 ** 0.282 **6. Peer Relations 0.369 ** 0.332 ** 0.220 ** 0.342 ** 0.372 **

7. Speech −0.114 −0.141 * −0.315 ** −0.127 −0.267 ** −0.177 **8. Syntax −0.137 * −0.180 ** −0.361 ** −0.106 −0.295 ** −0.201 ** 0.689 **

9. Semantic −0.198 ** −0.183 ** −0.398 ** −0.139 * −0.207 ** −0.291 ** 0.574 ** 0.617 **10. Coherence −0.316 ** −0.299 ** −0.338 ** −0.300 ** −0.350 ** −0.405 ** 0.543 ** 0.635 ** 0.690 **

11. Inappropriate initiation −0.429 ** −0.539 ** −0.302 ** −0.376 ** −0.448 ** −0.474 ** 0.351 ** 0.417 ** 0.523 ** 0.702 **12. Stereotyped language −0.382 ** −0.384 ** −0.346 ** −0.344 ** −0.402 ** −0.411 ** 0.444 ** 0.523 ** 0.597 ** 0.708 ** 0.704 **

13. Use of context −0.362 ** −0.319 ** −0.433 ** −0.283 ** −0.432** −0.536 ** 0.536 ** 0.612 ** 0.637 ** 0.768 ** 0.696 ** 0.734 **14. Nonverbal communication −0.332 ** −0.400 ** −0.256 ** −0.349 ** −0.462 ** −0.528 ** 0.454 ** 0.493 ** 0.478 ** 0.663 ** 0.647 ** 0.677 ** 0.750 **

15. Social −0.402 ** −0.407 ** −0.260 ** −0.404 ** −0.541 ** −0.676 ** 0.335 ** 0.389 ** 0.459 ** 0.623 ** 0.625 ** 0.620 ** 0.708 ** 0.755 **16. Interests −0.328 ** −0.378 ** −0.202 ** −0.305 ** −0.350 ** −0.455 ** 0.250 ** 0.297 ** 0.444 ** 0.584 ** 0.716 ** 0.605 ** 0.610 ** 0.601 ** 0.650 **

Note. 1–6 are the Conners behaviour scales and 7–16 are the CCC-2 communication scales. The correlations including the CCC-2 measures exclude participants for whom the CCC-2ratings were identified as invalid due to disproportionately positive or negative responses. N = 254 for correlations within the behaviour subscales, except for correlations withinattention (N = 253). N = 230 for all correlations with the communication subscales, except for inattention with communication (N = 229). All correlations with stereotyped languagehad N = 228, with the exception of the correlation with inattention which had N = 227. * denotes significance at the 0.05 level; ** denotes significance at the 0.01 level, two-tailed.

Table 4. Correlations between behaviour ratings and literacy measures.

Measure 1 2 3 4 5 6 7 8 9

1. Inattention2. Hyperactivity/impulsivity 0.573 **

3. Learning problems 0.324 ** 0.172 **4. Executive function 0.596 ** 0.419 ** 0.330 **

5. Aggression 0.338 ** 0.530 ** 0.197 ** 0.282 **6. Peer Relations 0.369 ** 0.332 ** 0.220 ** 0.342 ** 0.372 **

7. Reading 0.008 −0.022 −0.554 ** −0.041 −0.094 −0.0028. Spelling −0.050 −0.038 −0.543 ** −0.103 −0.094 −0.114 0.741 **

9. Vocabulary −0.032 0.009 −0.343 ** 0.088 −0.123 −0.074 0.450 ** 0.325 **10. Phonological Alliteration −0.010 0.027 −0.311 ** −0.039 −0.032 0.005 0.437 ** 0.301 ** 0.437 **

Note. 1–6 are the Conners behaviour scales and 7–10 are the literacy measures. The sample size for the behaviour scales is as in Table 4. The sample sizes for the literacy measures wereas follows. Vocabulary N = 250; spelling N = 251, except for with vocabulary (N = 247); reading N = 253, except for with vocabulary (N = 249) and spelling (N = 250); alliterationN = 251 except for with vocabulary (N = 247), spelling (N = 249), and reading (N = 250). * denotes significance at the 0.05 level; ** denotes significance at the 0.01 level, two-tailed.

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Table 5. Correlations between literacy measures and communication subscales.

Measure 1 2 3 4 5 6 7 8 9 10 11 12 13

1. Reading2. Spelling 0.743 **

3. Vocabulary 0.461 ** 0.320 **4. Phonological Alliteration 0.429 ** 0.274 ** 0.426 **

5. Speech 0.353 ** 0.336 ** 0.335 ** 0.233 **6. Syntax 0.414 ** 0.358 ** 0.438 ** 0.311 ** 0.689 **

7. Semantic 0.368 ** 0.302 ** 0.363 ** 0.154 * 0.574 ** 0.617 **8. Coherence 0.236 ** 0.225 ** 0.288 ** 0.105 0.543 ** 0.635 ** 0.690 **

9. Inappropriate initiation 0.136 * 0.145 * 0.193 ** 0.029 0.351 ** 0.417 ** 0.523 ** 0.702 **10. Stereotyped language 0.173 ** 0.203 ** 0.265 ** 0.044 0.444 ** 0.523 ** 0.597 ** 0.708 ** 0.704 **

11. Use of context 0.287 ** 0.297 ** 0.362 ** 0.125 0.536 ** 0.612 ** 0.637 ** 0.768 ** 0.696 ** 0.734 **12. Nonverbal communication 0.073 0.112 0.157 * −0.007 0.454 ** 0.493 ** 0.478 ** 0.663 ** 0.647 ** 0.677 ** 0.750 **

13. Social 0.076 0.123 0.162 * −0.073 0.335 ** 0.389 ** 0.459 ** 0.623 ** 0.625 ** 0.620 ** 0.708 ** 0.755 **14. Interests 0.077 0.093 0.082 −0.152 * 0.250 ** 0.297 ** 0.444 ** 0.584 ** 0.716 ** 0.605 ** 0.610 ** 0.601 ** 0.650 **

Note. The correlations including the CCC-2 measures exclude participants for whom the CCC-2 ratings were identified as invalid due to disproportionately positive or negativeresponses. The correlations with literacy here thus only include participants with valid CCC-2 ratings. * denotes significance at the 0.05 level; ** denotes significance at the 0.01level, two-tailed.

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3.4. Exploratory Factor Analyses

Tables 6–8 show the component matrices for parent ratings of behaviour and communication,and the literacy measures respectively. In all factor analyses, eigenvalues below 0.40 were suppressed.

Table 6. Exploratory factor analysis on the Conners behaviour subscales.

Behaviour Measures Factor 1

Inattention 0.783Hyperactivity/impulsivity 0.707

Executive Functions 0.664Aggression 0.554

Peer Relations 0.517Learning Problems

Note. Factor loadings lower than 0.4 are not shown.

Table 7. Exploratory factor analysis on the CCC-2 communication subscales.

Communication Measures Factor 1 Factor 2

Interests 0.892Social 0.838

Inappropriate Initiation 0.835Nonverbal 0.749

Stereotyped language 0.682Use of context 0.659

Coherence 0.553 0.423Syntax 0.856Speech 0.814

Semantics 0.579

Note. Factor loadings lower than 0.4 are not shown.

Table 8. Exploratory factor analysis on the literacy measures.

Literacy Measures Factor 1

Reading 0.950Spelling 0.712

Vocabulary 0.528Alliteration 0.505

Note. Factor loadings lower than 0.4 are not shown.

A one-factor solution emerged for the behaviour ratings, which explained 37.94% of the variance.The Inattention and Hyperactivity subscales loaded most highly on this factor, with moderate loadingsof Executive Function, Aggression and Peer Relations. The Learning Problems subscale was excludedas it did not have a sufficiently high loading.

A two-factor solution emerged for the communication scale. The six subscales measuringpragmatic and social communication loaded on Factor 1, which accounted for 59.71% of thevariance. Three of the four subscales tapping structural communication skills loaded on Factor 2,explaining 9.03% of the variance. Factor 1 was therefore linked with pragmatic and social aspects ofcommunication, and Factor 2 with structural communication skills. The Coherence variable loaded onboth factors (Factor 1= 0.553; Factor 2 = 0.423), reflecting its sensitivity to both pragmatic and structuralcommunication problems [16,58].

For the direct measures of literacy, a one-factor solution emerged that explained 48.56% of thevariance. Reading and Spelling loaded most highly on this factor, with moderate loadings fromVocabulary and Phonological Alliteration.

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3.5. Correlations between Factor Scores

The behaviour factor was strongly negatively associated with both the pragmatic (r = −0.617,p < 0.001) and structural (r = −0.322, p < 0.001) communication factors, indicating that childrenwith more behavioural problems had poorer communication skills (see Table 9 and Figure 1).The relationship between behaviour problems and pragmatic communication skills was significantlystronger than the association between behaviour and structural communication skills (Meng’sZ = −6.255, p < 0.001). In line with this, there was no relationship between the behaviour factorand direct measures of language structure as captured by the literacy factor (r = −0.097, p > 0.14).

Table 9. Correlations between factor scores.

Factor 1 2 3

1. Behaviour Factor2. Literacy Factor −0.091

3. Pragmatic and Social Communication Factor −0.617 ** 0.168 *4. Structural Communication Factor −0.322 ** 0.456 ** 0.656 **

Note. These correlations were unchanged when controlling for children’s age in months. * denotes significanceat the 0.05 level; ** denotes significance at the 0.01 level, two tailed.

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3.5. Correlations between Factor Scores

The behaviour factor was strongly negatively associated with both the pragmatic (r = −0.617, p < 0.001) and structural (r = −0.322, p < 0.001) communication factors, indicating that children with more behavioural problems had poorer communication skills (see Table 9 and Figure 1). The relationship between behaviour problems and pragmatic communication skills was significantly stronger than the association between behaviour and structural communication skills (Meng’s Z = −6.255, p < 0.001). In line with this, there was no relationship between the behaviour factor and direct measures of language structure as captured by the literacy factor (r = −0.097, p > 0.14).

Table 9. Correlations between factor scores.

Factor 1 2 3 1. Behaviour Factor 2. Literacy Factor −0.091

3. Pragmatic and Social Communication Factor −0.617 ** 0.168 * 4. Structural Communication Factor −0.322 ** 0.456 ** 0.656 **

Note. These correlations were unchanged when controlling for children’s age in months. * denotes significance at the 0.05 level;** denotes significance at the 0.01 level, two tailed.

Figure 1. Scatterplots of the correlations between the pragmatic and structural communication factors and behaviour problems.

Literacy was significantly related to both structural (r = 0.455, p < 0.001) and pragmatic (r = 0.152, p < 0.05) communication factors, indicating that children with better performance on the direct measures of structural language had better parent-reported communication skills. The association between literacy and structural communication skills was significantly stronger than the association between literacy and pragmatics (Meng’s Z = −5.747, p < 0.001), indicating that the direct assessments of literacy shared more variance with the parent ratings of structural language in communication (see Figure 2). These patterns of association were unaffected by controlling for age.

Figure 1. Scatterplots of the correlations between the pragmatic and structural communication factorsand behaviour problems.

Literacy was significantly related to both structural (r = 0.455, p < 0.001) and pragmatic (r = 0.152,p < 0.05) communication factors, indicating that children with better performance on the directmeasures of structural language had better parent-reported communication skills. The associationbetween literacy and structural communication skills was significantly stronger than the associationbetween literacy and pragmatics (Meng’s Z = −5.747, p < 0.001), indicating that the direct assessmentsof literacy shared more variance with the parent ratings of structural language in communication(see Figure 2). These patterns of association were unaffected by controlling for age.

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Figure 2. Scatterplots of the correlations between the pragmatic and structural communication factors and literacy.

4. Discussion

This study explored associations between the behavioural symptoms of ADHD and pragmatic and structural language abilities in a heterogeneous sample of children receiving support for problems in attention, learning, or memory. A bottom-up data driven approach identified dimensions of behaviour and language characterising the sample. This yielded a single dimension of behavioural problems that included inattention, hyperactivity and other behaviour problems commonly associated with ADHD. Although symptoms of inattention and hyperactivity can be diagnostically separate [60], it was not possible to differentiate them in the current sample. Three related dimensions of language emerged. One captured pragmatic communication skills and two encompassed children’s use of language structure. These were structural communication and literacy. Behaviour problems were strongly associated with pragmatic aspects of language, but less so with structural communication skills and not at all with literacy.

These differences in the relationship between the pragmatic and structural aspects of language function and behaviour are consistent with the idea that language impairments may have different sources [22,25]. Co-occurring behaviour difficulties and pragmatic communication problems may be underpinned by a common deficit in executive functioning. Pragmatic skills such as taking turns in conversation and not talking excessively, and the ability to control hyperactive/impulsive behaviours may both rely on hot executive skills like self-regulation and inhibition [2,37]. Likewise, features of social interaction such as monitoring and maintaining appropriate topics of conversation, and planning coherent speech, may draw on the same cool executive functions needed to maintain focussed attention (e.g., working memory) [61]. Consistent with this interpretation, executive function problems were present in the behaviour ratings in our sample. An alternative explanation is that there is a direct link between poor behaviour and weak pragmatic skills. By this account, difficult behaviour might directly limit opportunities for social interaction at home or school, impairing the development of social language skills [24,38]. Our sample had problems with peer relationships, signalling that they may indeed have had fewer opportunities to practice or develop pragmatic language skills.

Impairments in language structure may arise from different or additional sources to pragmatic and behavioural problems. Consistent with this, there was a weaker association between structural communication and behaviour than between pragmatics and behaviour. Moreover, literacy was unrelated to behaviour. This was unexpected given previous evidence linking ADHD symptoms, and in particular inattentive behaviour, with language and reading abilities [41,49]. One possibility is that the cognitive deficits limiting the acquisition and development of linguistic knowledge and skills are

Figure 2. Scatterplots of the correlations between the pragmatic and structural communication factorsand literacy.

4. Discussion

This study explored associations between the behavioural symptoms of ADHD and pragmatic andstructural language abilities in a heterogeneous sample of children receiving support for problems inattention, learning, or memory. A bottom-up data driven approach identified dimensions of behaviourand language characterising the sample. This yielded a single dimension of behavioural problemsthat included inattention, hyperactivity and other behaviour problems commonly associated withADHD. Although symptoms of inattention and hyperactivity can be diagnostically separate [60],it was not possible to differentiate them in the current sample. Three related dimensions of languageemerged. One captured pragmatic communication skills and two encompassed children’s use oflanguage structure. These were structural communication and literacy. Behaviour problems werestrongly associated with pragmatic aspects of language, but less so with structural communicationskills and not at all with literacy.

These differences in the relationship between the pragmatic and structural aspects of languagefunction and behaviour are consistent with the idea that language impairments may have differentsources [22,25]. Co-occurring behaviour difficulties and pragmatic communication problems may beunderpinned by a common deficit in executive functioning. Pragmatic skills such as taking turns inconversation and not talking excessively, and the ability to control hyperactive/impulsive behavioursmay both rely on hot executive skills like self-regulation and inhibition [2,37]. Likewise, features ofsocial interaction such as monitoring and maintaining appropriate topics of conversation, and planningcoherent speech, may draw on the same cool executive functions needed to maintain focussed attention(e.g., working memory) [61]. Consistent with this interpretation, executive function problems werepresent in the behaviour ratings in our sample. An alternative explanation is that there is a directlink between poor behaviour and weak pragmatic skills. By this account, difficult behaviour mightdirectly limit opportunities for social interaction at home or school, impairing the development ofsocial language skills [24,38]. Our sample had problems with peer relationships, signalling that theymay indeed have had fewer opportunities to practice or develop pragmatic language skills.

Impairments in language structure may arise from different or additional sources to pragmaticand behavioural problems. Consistent with this, there was a weaker association between structuralcommunication and behaviour than between pragmatics and behaviour. Moreover, literacy wasunrelated to behaviour. This was unexpected given previous evidence linking ADHD symptoms,and in particular inattentive behaviour, with language and reading abilities [41,49]. One possibility

Brain Sci. 2016, 6, 50 13 of 17

is that the cognitive deficits limiting the acquisition and development of linguistic knowledge andskills are different to the executive function problems that are affecting behavioural control andsocial communication in our sample. These additional or alternative deficits might include problemswith phonological processing. Supporting this idea, in the current study children’s phonologicalawareness and abilities in reading and spelling were strongly associated, but there was no link betweentheir behavioural attention problems and phonological skills. Phonological processing skills areimportant for literacy development [14] and difficulties with phonological processing influence theacquisition of letter-sound correspondences that are important for learning to read [27,40]. Phonologicalprocessing impairments are commonly observed in children with SLI who have structural languageimpairments [12]. However, children with elevated symptoms of ADHD or pragmatic languagedifficulties tend to have intact phonological processing skills unless they have co-morbid problemswith language structure [62,63], suggesting phonological deficits may be more closely associated withbroader structural language problems than pragmatic difficulties.

There were stronger links between the parent-reported measures of language and behaviour thanbetween parent-rated behaviour and the direct tests of literacy. This raises the possibility that theassociations between parent-rated communication and behaviour simply reflect common variance insubjective reports from parents/carers of children who are receiving support from professional services.Although we cannot rule out this possibility, several features of the data suggest the parent ratingsprovided meaningful measurements of children’s behaviour and language skills. Firstly, the parentratings of communicative language were related to the standardised literacy assessments, with astronger relationship between parent-rated structural communication and direct literacy measuresthan between pragmatic communication and literacy. Second, these parent-rated communicationscores similarly showed different strengths of association with parents’ behaviour ratings. Finally,parents’ views of their children’s learning abilities, as measured by a subscale of the behaviour checklist,correlated with the direct measures of literacy despite there being no other relationships between thesemeasures and other scales on the behaviour checklist. Taken together, the specificity of these linksspeaks against a common variance in the parent measures underpinning the results.

5. Conclusions

In summary, the phenotype of these children with problems in attention, learning or memorywas characterised by a broad dimension of inattentive and hyperactive behaviour that was stronglyassociated with pragmatic language difficulties, and more weakly associated with difficulties in theuse of language structure. The comorbidities between behavioural symptoms and pragmatic languageproblems may reflect a cluster of developmental problems underpinned by deficits in executivefunction difficulties [2], while problems with language structure may arise through difficulties inphonological processing. From a practical perspective, these findings suggest that different profilesof language impairment may require different intervention approaches. Pragmatic communicationproblems may benefit from behavioural interventions, such as psychosocial therapy or executivefunction-based interventions [64,65]. Approaches targeting other cognitive difficulties, such asphonological weaknesses [66] might be more beneficial than behavioural interventions for problems inlanguage structure.

Acknowledgments: The Centre for Attention Learning and Memory (CALM) research clinic at the MRC Cognitionand Brain Sciences Unit in Cambridge (CBSU) is supported by funding from the Medical Research Council ofGreat Britain to Duncan Astle, Susan Gathercole and Tom Manly. The clinic is led by Joni Holmes and managedby Francesca Woolgar. Data collection is assisted by a team of PhD students and researchers at the CBSU thatincludes Joe Bathelt, Sally Butterfield, Amy Johnson, Sinead O’Brien, Sara Gharooni, Sarah Bishop, Laura Forde,Agnieszka Jaroslawska, Erica Bottacin and Gemma Crickmore. The authors wish to thank the many professionalsworking in children’s services in the South-East and East of England for their support, and to the children andtheir families for giving up their time to visit the clinic.

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Author Contributions: E.H., J.H., D.A. and S.G. conceived the study; the CALM team collected the data; E.H.and J.H. analysed the data; E.H., J.H., D.A., and S.G. interpreted the data; E.H. and J.H. wrote the manuscript withimportant revisions and support from D.A. and S.G.

Conflicts of Interest: The authors declare no conflicts of interest.

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